Prism adaptation in the rehabilitation of patients with visuo

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WCO 18546
Prism adaptation in the rehabilitation of patients with
visuo-spatial cognitive disorders
Laure Pisellaa,b, Gilles Rodea,b,c,d, Alessandro Farnèa,b,
Caroline Tiliketea,b and Yves Rossettia,b,c,d
Purpose of review
The traditional focus of neurorehabilitaion has been on the
patients’ attention on their deficit, such that they should
become aware of their problems and gain intentional control
of compensatory strategies (descending approach). We
review prism adaptation as one of the approaches that
emphasizes ascending rather than descending strategies to
the rehabilitation of visuo-spatial disorders. The clinical
outcome of prism adaptation highlights the need for a
theoretical reconsideration of some previous stances to
neurological rehabilitation.
Recent findings
Recent years have given rise to a growing body of
experimental studies showing that the descending strategy
is not always optimal, especially when higher-level cognition
is affected by the patients’ condition. Ascending
approaches have, for example, used visuo-manual
adaptation for the rehabilitation of visuo-spatial deficits.
A simple task of pointing to visual targets while wearing
prismatic goggles can produce remarkable improvements
of various aspects of unilateral neglect.
Summary
The neural mechanisms underpinning visuo-manual
plasticity can be viewed as a powerful rehabilitation tool that
produces straightforward effects not only on visual and
motor parameters, but on visuo-spatial, attentional and
higher cognitive neurological functions. The use of prism
adaptation therapy in neglect and other visuo-spatial
disorders has just started to reveal its potential, both at a
practical and theoretical level.
Keywords
neglect, prism adaptation, rehabilitation, visuo-spatial
Curr Opin Neurol 19:000–000. ß 2006 Lippincott Williams & Wilkins.
a
INSERM, U 534, Espace et Action, Bron, France, bUniversité Claude Bernard
Lyon I, Lyon, France, cHôpital Henry Gabrielle, Hospices Civils de Lyon, Route de
Vourles, St Genis Laval, France and d‘Mouvement et Handicap’ Plateforme IFNLHCL, Institut Fédératif des Neurosciences de Lyon, Hospices Civils de Lyon, Lyon,
France
Correspondence to Y. Rossetti, INSERM U534, Espace et Action, Institut National
de la Santé et de la Recherche Médicale, Université Claude Bernard and Hospices
Civils de Lyon, 16 avenue Lépine, Case 13, 69676 Bron, France
Tel: +33 472 91 34 00; fax: +33 472 91 34 01; e-mail: [email protected]
Sponsorship: This work was supported by the INSERM AVENIR grant R05265CS,
Hospices Civils de Lyon, Université Claude Bernard and Programme Hospitalier de
Recherche Clinique.
Current Opinion in Neurology 2006, 19:000–000
Abbreviation
PPC
posterior parietal cortex
ß 2006 Lippincott Williams & Wilkins
1350-7540
Introduction
A large proportion of right-hemisphere stroke patients
show unilateral neglect. This is a multifaceted neurological deficit potentially affecting perception, attention,
representation and/or motor control within their leftsided space [1–3,4], as well as the right-sided hemispace
[5,6,7], inducing many functionally debilitating effects
on everyday life, and is responsible for poor functional
recovery and ability to benefit from treatment [8–10].
The various manifestations of unilateral neglect share
one major feature – patients remain unaware of the
deficits they exhibit or at least fail to fully consciously
attend to these deficits. This lack of awareness is
dramatically expressed in anosognosia and hemiasomatognosia [1]. It is therefore astonishing that the first
methods proposed for neglect rehabilitation were mainly
based on leftward voluntary orienting of attention. This
paradox was already underlined by Diller and Weinberg
([11], p. 67): ‘The first step in the treatment of hemiinattention is to make the patient aware of the problem.
This is particularly difficult in hemi-inattention since this
failure in awareness appears to be at the heart of the
patient’s difficulty’. It may indeed appear paradoxical to
base a rehabilitation procedure on awareness and intention in patients with a deficit in consciousness. Accordingly, these techniques have produced significant results,
but are clearly exposed to several limitations, i.e. the
voluntary monitoring of attention is restricted to a specific
context and does not apply as soon as more automatic
control is required.
To act on higher-level cognition in such a way as to
bypass the impaired conscious awareness and intention
one should, at least in principle, find another entry route
to space representation systems. Rubens [12] pioneered
such an ascending alternative, both theoretically and
experimentally, by providing preliminary support to
the prediction made by Jeannerod and Biguer [13]: a
unilateral lesion would produce an illusory displacement
1
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2 Trauma and rehabilitation
Figure 1 Prism adaptation in neglect
(a) Neglect patients adapt more than normals. In the pre-adaptive test, neglect patients exhibit a manual straight-ahead demonstration shifted to the
right with respect to normals. In the post-test, they reveal larger after-effects (redrawn from [15]). (b) Two examples of pre, immediate post and late
(þ2 h) performance of copy drawing.
of the egocentric reference, somewhat as if the subject
felt being constantly rotated toward the lesion side.
Rubens reported that vestibular stimulation, obtained
by pouring cold water into the neglect patients’ left
ear, instantly produced a dramatic, although transient
improvement of neglect.
Cognitive effects of prism adaptation
Both approaches to neglect rehabilitation have, however,
important limitations either in terms of absence of generalization (descending approach) or in terms of very limited duration (ascending approach) of the beneficial
effects. It was therefore a challenge to develop a strategy
to combine the advantages of the two approaches and to
propose a technique that, bypassing the awareness level,
could also promote long-lasting effects. Adaptation to
wedge prisms is a simple way of producing low-level,
automatic modifications of visuo-motor correspondences,
demonstrated by the presence of measurable after-effects
after the prism-exposure phase (Fig. 1a). In contrast to
more complex visual reorganization requiring extended
exposure [14], adaptation to wedge prisms has long been
known to quickly develop over the course of a 5-min
simple pointing session. Despite over 100 years of studies, only visuo-motor after-effects had been described
until the discovery that prism adaptation (prism adaptation) can improve higher cognitive deficits such as
unilateral neglect [15] (Fig. 1b).
The principles of prismatic adaptation
When someone first looks through wedge prisms that
optically displace the visual field, e.g. 108 in the rightward
direction, he/she may have little feeling that anything is
out of the ordinary, until he/she experiences extraordinary difficulty in perceptual-motor tasks (i.e. direct
effects of prism exposure). For example, pointing toward
a visual target produces an error to the right of the target
position. First, a relatively abrupt reduction of the lateral
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Prism adaptation Pisella et al. 3
Figure 2 Prism adaptation procedure
A proper prism adaptation session should include three periods: pre-tests, prism exposure and post-tests. During the early phase of the exposure, error
reduction (mainly accounted for by the strategic component) does not imply that prism adaptation is already effective. The post- and pre-tests, optimally
performed with nonexposed targets, are used to compute the amount of after-effect, i.e. proper adaptation.
error can be observed due to a strategic component of
adaptation. Then, a more gradual reduction of the terminal error is observed, returning to pre-exposure levels as
the person makes repeated attempts at target pointing.
Whereas the strategic component is at work only over a
short period of time [16], the true adaptation to the
prismatic displacement (or realignment) develops more
gradually and is more purely expressed during the subsequent slow phase of error reduction. When the prisms
are removed the person experiences unforeseen errors in
the opposite direction, to the left of the target! This
negative after-effect of prism exposure demonstrates
persistence of the adaptation acquired during exposure.
In most of our studies sham goggles were (and should be)
used to control for the spurious effects due to directional
visuo-motor activity. They were made of two pairs of 58
prisms producing opposite shifts, i.e. a total shift of 08
(same weight and same opacity as the 108 prisms). The
real and sham prisms were fitted into glacier goggles
(Cébé) in order to prevent any access to unshifted vision
(Optique Peter, Lyon, France; www.optiquepeter.com).
Vision of the starting hand position is usually occluded to
ensure the optimal development of the adaptation [17]. A
pointing task without visual feedback (open loop) is
performed before and after the adaptation procedure to
evaluate the development of a visuo-manual adaptation
to the visual shift.
Thus, the basic prism adaptation procedure simply
involves (1) pre-exposure baseline measurement of
pointing performance, (2) active exposure to prismatic
displacement to produce adaptation and (3) post-
exposure after-effect measurement of adaptation persistence (Fig. 2). Is this all there is to prism adaptation? Prism
adaptation may misleadingly appear simple when compared to the profound effects it can exert on spatial
cognition.
Generalization
Logically, the effects of prism adaptation should be
restricted to, or at least be best for, visuo-motor tasks,
because they share more common features with the
visuo-manual adaptation procedure. In the original study,
we observed the best improvement for the Schenkenberg
bisection test (6/6 patients markedly improved), whereas
the weakest improvement was obtained for text reading
(2/6 patients markedly improved) [15]. Many of the
therapeutic effects described since actually involved a
visual or a manual component, which may be directly
affected by the visuo-manual adaptation procedure [18].
It was therefore of prime interest to investigate the
possibility that prism adaptation could also improve
symptoms of unilateral neglect that may not be directly
affected by the adaptation (Fig. 3) and many other
neglect symptoms were therefore investigated (reviewed
in [19–21]).
The level of space representation assessed by mental
imagery tasks, for example, clearly differs from the sensory-motor level that is directly involved in the prism
adaptation procedure. Rode et al. [22,23] explored the
effect of prism adaptation on visual imagery and found
clear-cut improvements in neglect patients who initially
could not evoke city names on the western half of an
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4 Trauma and rehabilitation
Figure 3 A variety of therapeutic effects
(a) Reading performance before and after prism adaptation. The delineated area depicts the area that was correctly read by the patient. (b) Mental
imagery task performed before and after prism adaptation. The patient was asked to imagine the map of France and then to name as many cities he
could see on this internal map. The mental path followed the lines from 1 to the total number of cities. The dot and whiskers indicate the average location
and horizontal extent of this internal scanning (redrawn from [22]) (c) Postural control before and after prism adaptation. The sagittal position of the
centre of mass was recorded for 50 s (redrawn from [32]) (d) Writing under dictation before and after prism adaptation. The patient performance is
shown together with his daisy drawing from memory (from [71]). (e) Wheelchair driving before and after prism adaptation. Clockwise and, in particular,
counter-clockwise directions of driving were improved by prism adaptation (from [31]).
internally generated map of France. This result strongly
suggests that the after-effects of visuo-manual adaptation
are not restricted to visual and motor parameters. In the
same vein, Farné et al. [24] compared the effects of prism
adaptation in six neglect patients on both (1) visuo-motor
tasks, such as line and bell cancellation, and two subtests
taken from the Behavioral Inattention Test (letter cancellation and line bisection) battery, and (2) visuo-verbal
tasks (the visual scanning test, also taken from the
Behavioral Inattention Test, requiring a verbal description of the objects depicted on a colored picture, an
object-naming task with 30 Snodgrass pictures of familiar
objects intermingled with geometric shapes as distractors,
word and nonword reading). They observed that both
types of tasks followed a parallel improvement, which
lasted for at least 24 h.
The fact that different tasks based upon other sensory
modalities can be improved (haptic circle centering
[25–27]) and that several nonmanual tasks (postural
control, wheelchair driving, imagery, verbal reports) were
also improved, demonstrates that the effects of prism
adaptation on visuo-spatial defective abilities go well
beyond the visuo-manual parameters usually affected
in normal subjects. Recently, Berberovic et al. [28] have
shown that even a nonspatial and nonmanual aspect of
neglect could be improved, i.e. temporal order judgment.
Furthermore, we recently described beneficial effects of
prism adaptation on a new feature of unilateral neglect
reported by Zorzi et al. [29]. They introduced a mental
number bisection test, whereby patients have to verbally
indicate the middle between two numbers (e.g. between
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Prism adaptation Pisella et al. 5
11 and 19) and found a bias towards larger numbers in
neglect patients, as if their ‘mental number line’ was
distorted (similar to what classically occurs in line bisection). Even for this abstract task, we found that prism
adaptation strongly improved the bisecting bias [30].
Overall, these results make clear that adaptation to wedge
prisms affects a core component of unilateral neglect’s
complex spatial deficits.
Although generalization beyond purely visuo-motor tasks
is crucial for any putative rehabilitation technique, the
plasticity triggered by prism adaptation also produces
effects on nontrained tasks in the motor domain, such
as wheelchair driving [31] and postural control [32]. Such
effects are presumably mediated via spatial cognition
levels. In addition, the intentional component of neglect
deficits can also be improved by prism adaptation [18,33].
In this case, patients where asked to reach and grasp a
centrally located ball, and then to throw it into a left- or
right-sided basket. The kinematics of the centrally
directed reach-to-grasp movements showed that neglect
patients are overall slower when the secondary movement is directed to the left [33]. After a short prism
adaptation session, this asymmetry was modified for
several movement parameters (reaction time, movement
time, peak velocity, time to peak velocity). The pattern
of result observed immediately after prism adaptation
even showed the reverse pattern – reach movements
were slower when the ball had to be thrown to the right.
Therefore, the intentional control of action can be modified by prism adaptation.
Still at a motor level, there are several qualitative observations that prism adaptation can improve the motor
behavior of patients in everyday life [25]. One of the
crucial questions raised by the observation of a strong and
sustained improvement of unilateral neglect by a single
short adaptation session is whether this plastic effect is
restricted to the acute phase of the deficit. In our original
study patients were tested between 3 weeks and
14 months poststroke [15]. We have now collected data
on a group of patients who were exposed to the adaptation procedure between 5 and 28 years poststroke, and
amazingly found comparable amounts of improvement
[20,21].
Duration
Retention over time is another crucial feature of any
rehabilitation method. The effects of a single prism
adaptation session (for repeated sessions, see below) last
much longer (at least 2 h) than for any other sensory
stimulations (about 15 min) reported to date. A group
of patients showed a sustained improvement 24 h after
the training session [24], but individual cases may exhibit
even longer-lasting amelioration of neglect, now demonstrated to last up to about 1 week (e.g. [25,34]). An
interesting feature of prism adaptation is that its cognitive
beneficial effects, although often present immediately
after adaptation, seem to develop over short periods of
time thereafter, thus lagging somewhat behind the lowerlevel after-effects. Indeed, delayed cognitive effects (i.e.
2–4 h after prism adaptation) tend to be stronger then
immediate ones (measured just after prism adaptation)
even in chronic patients [15,35]. Although prism adaptation has long been thought to give rise to short-lasting
after-effects in healthy subjects, recent investigations
showed that the unaware mode of prism exposure can
give rise to astonishingly stronger after-effects [36,37].
As suggested below, another clinical interest of prism
adaptation may be found in the repetition of adaptation
sessions.
Anatomo-functional hypothesis
The literature is somewhat controversial about the neural
structures involved in prism adaptation. On the one hand,
neuropsychological evidence historically suggested that
only cerebellar patients are impaired in prism adaptation
(e.g. [38], reviewed in [39]). On the other hand, recent
imaging data [40] have suggested that the human
posterior parietal cortex (PPC) contralateral to the adapted
arm is the only area activated during prism exposure.
More recently, we established that the superior parietal
lobule, which when damaged leads to impairment of
visuo-manual guidance (optic ataxia), is not crucially
involved in visuo-manual prism adaptation [41]. The
clinical effect of prism adaptation on visual neglect also
precludes that the inferior parietal lobule, at least in the
right hemisphere, could be crucial for adaptation to rightward prisms. Rather, neglect patients exhibit ‘hyperadaptation’, characterized by more robust and durable
after-effects [15,24,25,32,34,42]. A bilateral optic ataxia
patient also demonstrated a larger inter-manual transfer,
highlighting the cerebellum as the most likely neural
substrate of true adaptation, although the PPC may also
contribute to the strategic component. We therefore
proposed a simple model [41] in which the cerebellum
and the PPC are, respectively, specialized for the adaptive and strategic components of prism adaptation
(Fig. 4): if the lesion of the PPC reduces the strategic
component, adaptation would consequently be mostly
achieved by realignment processes (true adaptive component); hence, it would more likely to be stronger,
longer-lasting and having more potential to generalize.
Accordingly, neglect patients do not notice the alteration
resulting from the optical deviation and normal subjects
exhibit larger adaptive after-effects when the prismatic
deviation is not noticeable [36,43].
In a patient with a cerebellar lesion (including
the superior part of the dentate nucleus and mostly
the anterior lobe of the left cerebellar hemisphere) we
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6 Trauma and rehabilitation
Figure 4 An anatomo-functional model
(a) A patient with a bilateral posterior parietal cortex (PPC) lesion has been shown to produced normal after-effects [41]. (b) Lesion of the right
cerebellum impairs adaptation to right-shifting prisms, independent of the arm used [44]. (c) Positron emission tomography showed that both right
cerebellum and left hemisphere structures exhibited a blood flow increase correlated with neglect score improvement [48]. In (a–c) the amount of
adaptation found in these patients is indicated in black on the vertical bar and should be compared with a normal after-effect ranging from about 30–
50%. (d) According to the interhemispheric balance framework, neglect patients exhibit a bias to the left side (‘Pre’). We speculate that prism
adaptation acts at the cerebellar level and indirectly interferes with the left hemisphere, such that the balance is improved or restored (‘Post’).
found adaptation to be limited to a rightward (not
leftward) prism deviation, independent of the hand
used during exposure [44]. This observation led us to
confirm the crucial involvement of the cerebellum in
prism adaptation, and to propose a lateralized model
for prism adaptation and its beneficial effect on spatial
cognition. The pattern of impairment of this patient
suggested a visual lateralization within the cerebellum
with the involvement of the cerebellar hemisphere ipsilateral to the prismatic deviation in the processing of
visual errors, in addition to the well-known motor lateralization that involves mainly the cerebellar hemisphere
contralateral to the hand for the modification of the visuomotor correspondences [45]. To our knowledge, only one
other anatomo-functional study has compared, in monkeys, adaptation to right and left prismatic deviations
[46]. In this study, deficit in adaptation was observed after
inactivation of the ventral premotor cortical area only
when vision was shifted contralaterally to the inactivated
ventral premotor cortical area. Since connections
between the cerebellum and the cerebral cortex are
crossed [47], this makes a consistent cerebro-cerebellar
lateralized network for the computation and integration
of directional visual error in prism adaptation. The
implication of such a lateralized cerebello-cerebral network in the functional anatomy of the therapeutic effects
of prism adaptation on neglect has been recently confirmed by functional neuroimaging in neglect patients
[48] showing that the right cerebellar hemisphere
and the right dentate nucleus were both significantly
activated in the positive covariation analysis between
the prism adaptation-induced changes in regional
cerebral blood flow and in neuropsychological performance (assessed by the Behavioral Inattention Test).
The activation of the left temporal cortex also appeared
to covariate positively with the left spatial neglect
improvement [48].
Altogether, anatomical and behavioral data suggest that
the clinical effect of prism adaptation on neglect relies on
a network of brain areas where the visual error-signal
generated by right prisms is initially processed in the left
occipital cortex. The information is then transferred to
the right cerebellum where the visuo-motor realignment
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Prism adaptation Pisella et al. 7
(i.e. ‘true adaptation’) takes place in congruence with the
rightward deviation of prisms. The clinical effect could
be mediated through the modulation of cerebral areas in
the left hemisphere via a bottom-up signal generated by
the cerebellum [20,44,49]. Notably, the temporal cortex,
the frontal cortex and the PPC have been shown to be
targets of output from the cerebellum via a neuronal loop
also implicating the dentate nucleus and subcortical
structures, such as the thalamus and the globus pallidus
[50–52]. The clinical effect might therefore be mediated
by the recruitment of pathways in the left hemisphere
that are functionally homologous to those involved in
spatial cognition in the damaged hemisphere.
Reciprocally, the cognitive effects of prism adaptation
found in healthy subjects [53–55], demonstrated by an
asymmetrical pattern of performance on several spatial
tasks, are strictly dependent upon the direction of the
prismatic shift [49]. On the basis of the latter studies and
considering that the right parietal cortex seems to be
specifically involved in line bisection judgment tasks
[56–57], we hypothesized that the function of the right
parietal lobe would be inhibited by inputs from the left
cerebellar cortex, coherent with the use of the leftward
prismatic deviation, and create ‘neglect-like’ symptoms
[58].
In principle, the proposed model is compatible with the
involvement of the prism adaptation-induced realignment of the oculomotor system that, by reducing the
rightward scanning bias, may facilitate exploration of the
left neglected side of space [59,60,61]. Several dissociations have, however, been documented between
oculomotor change and the amelioration of visuo-spatial
behavioral performances [62,63]. Another proposal is that
adaptation acts through plastic modification of the integration of proprioceptive and visual information, which
would be particularly beneficial in neglect patients whose
symptoms result in part from an impaired visual-motor
mapping of space (see [64]). One could speculate that
prism adaptation permits an enlargement of this visualmotor mapping of space not only on the left side, but also
on the right side, as suggested by the improvement of
constructional apraxia [21] and spatial dysgraphia following prism adaptation. Recent findings mainly point to the
need for appropriately applying prism exposure conditions and quantification [18], for evaluating the role
played by the type of prism adaptation (strategic vs.
realignment; [59,60]), as well as the sufficient amount
of adaptation (as measured in terms of after-effect)
required to produce consistent neglect improvement
[65]. There is still the need to build up a coherent
framework integrating one century of prism adaptation
investigations with the recent body of patient literature
[66]. An interesting issue also remains to identify domainspecific aspects of neglect, such as chimeric face percep-
tion, which seem even intractable by prism adaptation
[35,63,67].
Conclusion
Adaptation to prismatic displacement is particularly suited for clinical application [38] because its incremental
nature permits examination over relatively short time
periods, in contrast to prismatic distortions like left–right
or up–down reversal of the visual field that require
extended exposure for adaptation to occur [68]. The
efficacy of single-session prism adaptation has proven
to generalize the improvement to several neglect symptoms. Several nonmotor as well as motor aspects of the
neglect syndrome, such as motor neglect and/or extinction, might actually benefit from prism adaptation as well.
It can be considered the most-promising rehabilitation
method for unilateral neglect to date [4,69], especially in
light of the fact that spontaneous recovery from neglect is
very limited [70]. We wish to put forward that prism
adaptation might improve spatial-cognition deficits in
neglect as well as in other pathologies. Constructional
deficits, dysgraphia [71], as well as spatial attention
distortions contributing not only to neglect [22,72,42],
but also to other pathological manifestations affecting
spatial and bodily representations [73] (e.g. Complex
Regional Pain Syndrome [74,75], are on the list of candidates for this bottom-up rehabilitation track. In spite of
these possibilities, it is now clear that not all neglect
patients can benefit from prism adaptation and not to the
same extent. Unfortunately, to our knowledge, only
one randomized controlled trial has been performed to
date [21]. In addition, several important questions still
await definitive answers: why is adaptation quantitatively
more important and lasts longer in patients vs. healthy
controls, why it affects higher-order cognitive domains,
why it is direction-specific and what are the predictors of
prism adaptation clinical efficacy? Beyond prism adaptation in and of itself, it is also promising to consider that
other original bottom-up approaches may prove to be
more effective on cognitive disorders than the traditional
top-down stance.
The practical clinical potential of repetitive-session
prism adaptation procedures has just begun to be
explored. Frassinetti et al. [76] reported that a group of
patients who benefited from two prism adaptation sessions daily over 2 weeks (a total of 10 sessions) exhibited
an improvement that lasted over 5 weeks after the end of
the treatment. A daily prism adaptation session has been
reported to improve neglect up to 3 months after treatment [60]. Long-standing chronic neglect (11 years) has
also been demonstrated to improve with repetitive prism
adaptation sessions [35]. Using the neck vibration technique and visual-scanning training, Schindler et al. [77]
also explored the effects of repetitive sessions, and found
a sustained improvement following an intensive daily
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8 Trauma and rehabilitation
programme. Obviously, such studies should be systematically undertaken to determine the optimal training
frequency and duration, as well as the optimal combination of techniques that can be used routinely for
rehabilitation [78].
20 Rode G, Pisella L, Rossetti Y, et al. Bottom-up transfer of visuo-motor
plasticity. Prism adaptation. Prog Brain Res 2003; 273–287.
Acknowledgements
23 Rode G, Rossetti Y, Boisson D. Prism adaptation improves representational
neglect. Neuropsychologia 2001; 39:1250–1254.
The authors wish to thank Dominique Boisson, Sophie JacquinCourtois, Jacques Luauté, Denis Pélisson, Claude Prablanc and Alain
Vighetto for fruitful discussions, and Stephanie Maxfield for her
comments on a previous version of this manuscript.
24 Farnè A, Rossetti Y, Toniolo S, Làdavas E. Ameliorating neglect with prism
adaptation: Visuo-manual vs visuo-verbal measures. Neuropsychologia 2002;
40:1069–1080.
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